SCIENCE ADVANCES | RESEARCH ARTICLE

ECOLOGY Copyright 2017

The Authors, some
rights reserved;
Networks of global bird invasion altered by exclusive licensee
American Association
regional trade ban for the Advancement
of Science. No claim to
original U.S. Government
Lus Reino,1,2,3 Rui Figueira,1,3,4 Pedro Beja,1,3 Miguel B. Arajo,2,5,6 Works. Distributed
Csar Capinha,1,7* Diederik Strubbe6,8,9 under a Creative
Commons Attribution
Wildlife trade is a major pathway for introduction of invasive species worldwide. However, how exactly wildlife NonCommercial
trade influences invasion risk, beyond the transportation of individuals to novel areas, remains unknown. We License 4.0 (CC BY-NC).
analyze the global trade network of wild-caught birds from 1995 to 2011 as reported by CITES (Convention on
International Trade in Endangered Species of Wild Fauna and Flora). We found that before the European Union
ban on imports of wild-caught birds, declared in 2005, invasion risk was closely associated with numbers of
imported birds, diversity of import sources, and degree of network centrality of importer countries. After the
ban, fluxes of global bird trade declined sharply. However, new trade routes emerged, primarily toward the
Nearctic, Afrotropical, and Indo-Malay regions. Although regional bans can curtail invasion risk globally, to

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be fully effective and prevent rerouting of trade flows, bans should be global.

INTRODUCTION
Global wildlife trade has attracted public attention in recent years be-
cause it is a major driver of species extinctions around the world (1, 2),
and because it helps promote the spread of invasive species (3) and of
diseases to both humans and other animals (4). Outright bans on
wildlife trade of both threatened and potentially damaging species have
been proposed as a strategy to reduce its negative effects (5). This
strategy can have major social and economic costs, so its effectiveness
needs to be thoroughly evaluated. Arguably, the most prominent
application of trade bans was enacted by the European Union (EU),
which placed a temporary ban on wild bird imports in October 2005
to prevent the spread of avian influenza (6). The ban was made perma-
nent in July 2007 and comprised all wild bird imports regardless of spe-
cies conservation status (7). Although supported by a coalition of
conservation and animal welfare organizations (8), the decision was cri-
ticized on the grounds that blanket trade bans would risk stimulating
illegal activities (9) and, when imposed by northern on southern con-
stituencies, run counter to values of equity and sustainable development
(10). Also, rather than reducing market demands, trade bans could lead
to the opening of alternative markets and trade routes, thus contributing
to spread of invasive species into areas otherwise disconnected from
major trade networks. The effectiveness of trade bans as a generic con-
1
CIBIO/InBIO-Centro de Investigao em Biodiversidade e Recursos Genticos,
Universidade do Porto, Campus Agrrio de Vairo, Rua Padre Armando Quintas,
n9, 4485-661 Vairo, Portugal. 2CIBIO/InBIO-Centro de Investigao em Biodiver-
sidade e Recursos Genticos, Universidade de vora, 7004-516 vora, Portugal.
3
CEABN/InBIO-Centro de Estudos Ambientais Prof. Baeta Neves, Instituto Superior
de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Portugal.
4
LEAF-Linking Landscape, Environment, Agriculture and Food, Instituto Superior de
Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Portugal.
5
Museo Nacional de Ciencias Naturales, CSIC, Calle Jos Gutirrez Abascal, 2,
28006 Madrid, Spain. 6Center for Macroecology, Evolution and Climate, Natural
History Museum of Denmark, University of Copenhagen, Universitetsparken 15,
2100 Copenhagen, Denmark. 7Zoologisches Forschungsmuseum Alexander Koenig,
Museumsmeile Bonn, Adenauerallee 160, 53113 Bonn, Germany. 8Terrestrial Ecology
Unit, Ghent University, K.L. Ledeganckstraat 32, 9000 Ghent, Belgium. 9Evolutionary
Ecology Group, University of Antwerp, Campus Drie Eiken, Universiteitsplein 1, 2610
Wilrijk, Belgium.
*Present address: Global Health and Tropical Medicine, Instituto de Higiene e
Medicina Tropical, Universidade Nova de Lisboa, Rua da Junqueira 100, 1349-
008 Lisboa, Portugal.
Corresponding author. Email: diederik.strubbe@snm.ku.dk
servation approach has been actively debated (11); although it is known
that gross metrics of international trade generally correlate with the
global distribution of invasive alien species (1214), exactly how trade
networks influence the success of biological invasions remains un-
known (15). However, this knowledge is key to effectively manage trade
networks in relation to their potential effects on global patterns of inva-
sive species establishment.
We assess how the topology of the global bird trade network relates
to the establishment of imported non-native bird species. We also in-
vestigate how the unilateral EU import ban on wild-caught birds has
changed the species traded, their traded volumes, and the network of
trading relationships and balance among countries. To do so, we com-
bine a large data set on wild bird trade among biogeographical realms
derived from CITES (Convention on International Trade in Endangered
Species of Wild Fauna and Flora) with the analysis of trade network
topology. Our focus on birds and the EU import ban is especially rele-
vant because the EU has been, historically, the main importer of wild
birds worldwide (16). Moreover, birds are among the most internation-
ally traded animal taxa (17), and highly traded avian orders such as
the Psittaciformes represent both the most threatened (18) and most
invasive (19) bird group. Results of our analysis have broader im-
plications to understand the links between trade networks and bio-
logical invasions, and thus to devise trade policies reducing invasion
risks.
RESULTS
Avian invasion success is related to global fluxes of wild-caught birds,
and as expected, countries that import more birds are more prone to
being invaded by birds (Table 1). In addition, a number of intrinsic
properties of the trade network topology also relate to invasion prob-
ability. Regardless of levels of bird importation, countries that have a
more diversified number of importation sources (that is, high indegree
centrality) are more likely to be invaded. The same is true for subgroups
of countries that form a dense interconnection of trading relationships
among themselves (that is, having a high clustering coefficient). Last,
invasion risks are higher for countries that have a more central position
in the whole trade network (that is, that have higher values for close-
ness centrality; see Table 1). Before the EU ban (19952005), trade in

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SCIENCE ADVANCES | RESEARCH ARTICLE

CITES-listed wild birds between biogeographical realms totalized ca.
1.3 million individuals annually.
The EU ban reduced trade volumes to about 10% of their former
levels while strongly redistributing the remaining trade flows across
the globe (Figs. 1 and 2 and table S1). Before the ban, trade volume
was the dominant invasion risk parameter for 59% of countries globally,
followed by closeness centrality (27%), clustering coefficient (8%), and
indegree (5%). Network parameters were especially influential across
Europe, North America, and parts of Latin America and Asia (fig. S1).
The EU bird trade ban reduced the importance of trade volume globally
(dominant in 47% of countries) and increased the contribution of
network parameters for explaining invasion success [closeness centrality
(27%), clustering coefficient (19%), indegree (6%); fig. S2]. In the period
19952005, European and North American countries were most central
to the global trade network. After the ban, the United States remained
among the most densely connected trading countries, whereas EU

Table 1. Relationships between trade network topology and avian invasion. The variable quantity refers to the total number of individual of the species
that were imported. Indegree describes the number of countries from which a country imports birds. Closeness centrality indicates how close a country is to all
other countries in the trade network. The eigenvector centrality measures the influence of a country in the trade network, whereas betweenness centrality
measures the role of countries as pass-through centers. The clustering coefficient quantifies the extent to which a country is integrated into a subgroup of
countries that have a highly interconnected trade network among themselves. Avian invasion success was best explained by the quantity of birds traded and by
having more closely connected trade networks [that is, high values for indegree centrality, closeness centrality, and the clustering coefficient; model deviance
information criteria (DIC) weight, 0.82; DDIC with the second-best model > 3]. Quantity and indegree centrality were also included in the second-best model, as
was betweenness centrality, but this model was only weakly supported (DIC weight, 0.16). All other models had virtually no support (all DIC weights 0.021).

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Variable DIC weights and posterior means and confidence intervals (CIs) support the relevance of the four variables included in the best-ranked model (all DIC
weights 0.82, 95% CI excluding 0). Heidelberger convergence diagnostics indicate that models reached stationarity.
Variable Posterior mean and CI Effective sample size MCMC P value DIC weight

Quantity 0.020 (0.0055 to 0.034) 1122.7 <0.001 1.00

Indegree 0.051 (0.028 to 0.076) 1424.7 <0.001 1.00

Closeness centrality 0.12 (0.066 to 0.17) 1624.9 <0.001 0.84

Clustering coefficient 0.040 (0.0066 to 0.076) 1855.2 0.033 0.84

Betweenness centrality 0.016 (0.024 to 0.056) 2869.0 0.45 0.18

Eigenvector centrality 0.030 (0.044 to 0.10) 1638.8 0.42 0.02

Fig. 1. Global wild bird trade fluxes. Flows of wild bird trade among different biogeographical regions, before (A) and after (B) the EU ban.

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SCIENCE ADVANCES | RESEARCH ARTICLE

member states were replaced by predominantly Asian nations and
South Africa (table S2). Overall, network parameter values were reduced
to 18 to 21% of their former levels (fig. S3), and this reduction was es-
pecially strong across the western Palearctic (table S3). Corresponding-
ly, overall avian invasion risks have decreased strongly across much of
the globe, and especially so in (western) Europe, where invasion risks
were the highest before the ban. Minor to moderate increases in inva-
sion risk attributable to rerouted trade flows are apparent especially in
the Nearctic and, to a lesser extent, in parts of the Indo-Malay and Afro-
tropical regions (Fig. 3 and figs. S4 and S5). Almost 90% of pre-ban trade
fluxes corresponded to imports into the western Palearctic, mainly
coming from the Afrotropical region, with secondary fluxes from the
Neotropical and Indo-Malayan regions (Fig. 1 and Tables 2 and 3).
Before the ban, a small set of countries was responsible for a large
share of global wild bird trade because, overall, about 66% of global bird
imports were made by only five EU countries (Belgium, Italy, Netherlands,
Portugal, and Spain), whereas three West African countries (Guinea,
about 75% belonged to 12 Afrotropical species, with the main trade
fluxes concentrated from West Africa to western Europe (fig. S6 and
tables S4 and S5). Parrots and allies (Psittaciformes) were the second
most traded group (17.5% of trade). As for passerines, main trade fluxes
were toward western Europe, but they came from a more varied range
of source countries across South and Central America, South Africa,
and Southeast Asia (fig. S7 and tables S4 and S5).
After the EU ban, exports toward the western Palearctic and exports
from the Afrotropical region were reduced to a mere 1.25% (Table 2)
and 4.34% (Table 3) of their pre-ban level, respectively. The Neotropical
region gained importance as a main source of wild birds, generating
over 50% of global wild bird exports (Table 3). The role of the EU as
the predominant bird importer shifted toward other regions, principally
to the Nearctic, and especially to Mexico and the United States, where
imports increased from over 23,000 to more than 82,000 birds annually
(Figs. 1 and 2, Table 2, and table S1). The Indo-Malay and Afrotropical
regions also gained (relative) importance in the global trade network,

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Mali, and Senegal) were responsible for more than 70% of bird exports because bird imports into countries such as Singapore and South Africa
(table S1). Most birds traded were passerines (almost 80%), of which declined less strongly than in the western Palearctic (59% and 17% of

Fig. 2. Annual number of birds exported to different biogeographical realms (19952011). Total annual numbers of imported birds (A), passerines (B), and parrots
and cockatoos (C). Color codes correspond to the different biogeographical regions depicted in Fig. 1 (light blue, western Palearctic; red, eastern Palearctic; yellow,
Indo-Malay; green, Nearctic; brown, Neotropical; dark blue, Afrotropical; pink, Australasia).

Fig. 3. Trade bandriven changes in avian invasion risk. Predicted changes in wild bird tradedriven invasion risk caused by the EU wild bird import ban. Country-
level invasion risk estimates were obtained by summing model invasion probabilities for all bird species exported to a given country in the pre-ban (19952005) versus
post-ban (20062011) period. Green and orange hues indicate decreases and increases in invasion risk, respectively; color gradients are on the same scales; and maps
have been drawn using equally spaced intervals. Invasion risks have most strongly declined across (western) Europe, whereas more moderate increases can be ob-
served across parts of the Nearctic and Indo-Malay regions.

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Table 2. Annual number of birds exported to different biogeographical realms before and after the 2005 EU ban.
Before the EU ban (19952005) After the EU ban (20062011)
Number of individuals Number of species Number of individuals Number of species

Western Palearctic 1,141,856 672 14,307 263

Eastern Palearctic 22,476 374 4,408 144

Indo-Malay 53,950 300 16,304 118

Nearctic 23,564 429 82,780 201

Neotropical 8,113 289 819 91

Afrotropical 49,433 342 10,438 154

Australasia 33 19 1 3

Not identified 302 48 2,245 87

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Total 1,299,729 806 131,340 422

Table 3. Annual number of birds exported from different biogeographical realms before and after the 2005 EU ban.
Before the EU ban (19952005) After the EU ban (20062011)
Number of individuals Number of species Number of individuals Number of species

Afrotropical 1,057,819 358 45,937 224

Western Palearctic 82,052 453 2,853 153

Neotropical 52,531 248 69,206 114

Indo-Malay 45,805 252 3,127 90

Eastern Palearctic 38,099 155 841 64

Nearctic 20,979 267 8,457 129

Australasia 2,187 40 810 13

Not identified 254 147 102 44

Total 1,299,729 806 131,340 422

pre-ban volumes, respectively; table S1). The taxonomic composition of
the trade also changed, because passerine birds are no longer the dom-
inant traded taxon (annual trade volumes in the period 20062011
amounted to only 2.40% of the pre-ban volume; tables S4 and S5). Parrot
trade declined as well (on average about 45% of its pre-ban volumes;
tables S4 and S5), although trade volumes had recovered to almost
60% of their pre-ban levels by 2011 (Fig. 2). Consequently, parrots are
now the most traded group (accounting for 78% of global annual trade),
followed by Passeriformes (at 19%).
DISCUSSION
We show how detailed characterization of trade networks can reveal the
strong connection between global trade pressure and success in
biological invasions. The drastic drop in the global number of birds (le-
gally) traded following the 2005 EU ban on bird trade underscores the
importance of internationally coordinated policies in conservation. The
number of birds traded is one of the most important factors in
determining avian invasion risk, and the EU bird trade ban has
effectively reduced global bird invasion risks. However, alternative trade
routes have opened since then, leading to potential increases in invasion
risks in countries that otherwise had remained relatively less affected by
bird invasions. Remaining trade flows have also been redirected toward
developing countries, mainly around the tropical belt where biodiversity
is high but resources to manage invasive species are limited (20).
Global changes in trade volumes, however, cannot alone predict the
magnitude, sometimes even the direction, of regional changes in invasion
risk. Network centrality measures are also needed to reliably predict in-
vasion risk. For example, in the Nearctic, exports to both Mexico and
the United States increased and yet invasion risk declined in the former
but increased in the latter (Fig. 3). This asymmetry seems to be a con-
sequence of the United States holding on to its central position in the
global trade network (indegree was largely stable, and closeness central-
ity and clustering coefficient increased; table S2 and figs. S1 and S2). In

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SCIENCE ADVANCES | RESEARCH ARTICLE
contrast, Mexicos influx of bird trade is largely driven by a strong in-
crease in imports of monk parakeet (Myiopsitta monachus), resulting in
increased invasion rates for this single species only (21). Whereas before
the EU ban, 47 countries exported 189 different bird species to Mexico,
after the ban, trade was limited to 13 countries exporting only 55 species,
and the country became more marginal to global trade network
(network centrality measures fell to 14 to 69% of their former levels;
table S2 and figs. S1 and S2). This interplay between trade volumes and
network centrality generates complex, regional dynamics in invasion risk,
necessitating the use of network models to obtain more realistic predictions
of how trade politics affect pathways and success of biological invasions.
East Asia is a region with a prominent culture of bird keeping and
strong economic development (22, 23), and as wild bird trade in the
region has declined to a lesser extent than globally, it has gained a more
prominent role in the global bird trade network. However, whereas our
results lead to predicting a decline in trade-driven invasion risk in parts
of East Asia, recent studies suggest that the rate of avian invasions in the
region is increasing (24, 25). This apparent discrepancy might be a con-
sequence of potential biases arising from the fact that here, we only con-
sider trade in wild-caught birds among biogeographical realms. Much of
the bird trade in East Asia involves either wild-caught birds that are native
to the Indo-Malay region or birds that have been bred in captivity (26, 27).
It should be noted that whereas captive breeding is common
across Indonesia (28), evidence strongly suggests that, for example,
in Singaporethe main regional bird trade hubmany of the birds
reported to CITES as captive-bred are in reality taken from the wild
(29, 30). Illegal wild bird trade likely is vast, but its trade routes and
volumes are difficult to quantify (31) and it remains unclear to what
extent illegal trade contributes to invasions globally. A recent review
on illegal parrot trade concluded that poached parrots are much more
likely to be sold on local markets within the biogeographical area of
capture than to be exported internationally (32). If this correlation holds
true for other bird taxa and biogeographical regions, this observation
suggests that birds invading localities within their biogeographical
region of origin should also be considered to detect signals of illegal
wildlife tradedriven avian invasion risks.
For many taxa, current rates of invasion may reflect historical, rather
than contemporary, human activities [termed invasion debts; (33)].
However, taxonomic groups with good dispersal capacities, such as
birds, are more strongly associated with recent socioeconomic drivers
(33). Four of six invasion events we uncovered in the post-ban period
refer to Portugal and Greece, where no legal wild bird imports took
place in that period and thus likely reflect such an invasion debt. The
low number of avian invasions attributable to post-ban wild bird trade
confirms that birds react rapidly to changes in factors underlying inva-
sion success, and demonstrates that trade bans are an effective means to
halt avian invasions.
An additional source of uncertainty comes from an increase in the
discrepancy between exporter- and importer-reported bird quantities
after the implementation of the ban (fig. S8). For example, increased
invasion risks in the United States partly depend on post-ban exports
of African passerines reported by Senegal but never recorded as imports
by the United States. These discrepancies are attributable to a range of
factors (34). For instance, exporters must obtain CITES documents
before the export, and because the process can take time, they may re-
quest permits before the birds are actually available for export. Occa-
sionally, documents may be issued for birds that are never exported
(35). When exporters report bird trade volumes larger than reported
by the importer, our models are likely to overestimate post-ban invasion
Reino et al., Sci. Adv. 2017; 3 : e1700783 22 November 2017
risks (fig. S8). Therefore, to better understand how shifting trade
patterns influence species introductions and invasion success, we re-
commend that implementations of graph theory can be used to inte-
grate CITES trade data with actual international trade statistics (for
example, see UN Comtrade, https://comtrade.un.org). Furthermore, fu-
ture assessments should take into account the environmental suitability
of the non-native area to which traded species are transported. These
assessments could be achieved through correlative modeling of climatic
similarities between native and invaded areas [for example, see the
studies of Thuiller et al. (12), Capinha et al. (14), and Cardador et al.
(36)]. However, predictions of environmental suitability assume perfect
transferability of realized niches, which is generally unlikely (37).
Changes in the shape and size of realized niches between native and
invaded ranges can result in both over- and underprediction of the
extent of area suitable for species establishment (38), so caution would
be required when interpreting the results of pooled network and
environmental suitability analyses. We note that our data set on suc-
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cessful bird invasions is dominated by parrot species and, to a lesser
extent, passerine invasions across Europe (table S6). This is to be
expected, because these are the two most traded bird taxa, the known
taxonomic bias in CITES-listed species and the pre-ban trade predom-
inance of bird imports into Europe (16).
In conclusion, trade bans unilaterally implemented by a major eco-
nomic power can effectively reduce species invasion risk globally. How-
ever, by definition of their regional nature, these bans cannot eliminate
trade-driven invasion risk fully. New, generally smaller trade routes
have opened since the European ban took place, driven by the availa-
bility of transport infrastructures and the vagaries of supply and demand
(39, 40). Although it remains to be seen how important the network
topology parameters identified here are for invasions of other taxa
and to other areas, our study highlights how network theory and tools
can be applied to quantify the probability of successful species invasions
via trade and transport networks. In particular, network models can be
used to identify countries or regions emerging as central to these newly
formed trade relations, where new invasions may thus be likely to occur.
Investing in better biosecurity, surveillance for likely high-risk invasive
species, and improved socioeconomic governance (20) in such countries
will enable the global community to more effectively prevent and mit-
igate future biological invasions.
MATERIALS AND METHODS
Experimental design
CITES trade data
Data on global bird trade between biogeographical realms were ob-
tained from the CITES database (available online at https://trade.cites.
org/). This database is maintained by the Secretariat of the CITES and
registers trade between signatory countries. The database holds trade
information on about 5600 animal species listed in the different CITES
Annexes, though it is not without limitations. First, it covers only 1700
of 2600 bird species known to be traded. World bird trade markets are
dominated by the trade in Passeriformes and Psittaciformes, and whereas
the latter are well characterized, the former are underrepresented (16).
Second, CITES relies on information communicated by governments
of exporter and importer countries, and data are, therefore, not free of
errors or biases. For example, there are chances that governments might
occasionally fail to correctly report transactions, that species might be
misidentified, and that the number of individuals involved might be
poorly estimated (34). Despite these potential errors and biases in the
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documentation of trade, CITES represents the only global, legally
binding, convention addressing international trade in wildlife in a
structured and verifiable manner, and it constitutes a valuable source
of information to assess the relationships between species invasions
and international trade.
Data were downloaded from the CITES database, using the global
checklist Catalogue of Life (www.catalogueoflife.org) as the taxonomic
authority. Queries on the database were performed at the genus level,
for the periods 19952005 (before the EU ban) and 20062011 (after the
EU ban), using the following criteria: live for trade term, all coun-
tries for export and import countries, wild for source of species,
and all purposes for purpose of trade transaction. We selected these
periods because by 1995, 75% of the parties had already signed the con-
vention, and data could be considered representative of general, global
trade patterns. Also, from 1995 onward, the accuracy of the database
improved by the implementation of taxonomic and species distribution
checks. The year of 2011 was chosen as the upper limit to allow for the
identification of successful establishment of introduced non-native
birds (see below) (41). Several database quality verification steps were
undertaken. First, duplicated data lines and records that equate import-
er and exporter countries were removed from the data set. Second, to
obtain the number of live wild birds traded in each transaction, we
followed the conservative approach recommended by the Guide of
the CITES Trade Database, by selecting the higher figure between the
quantity reported by the exporter and the importer. Third, we only re-
tained exporter-importer species transactions whereby the number of
individuals traded cutoff of five birds, because this cutoff represents
a >95% probability that both sexes have been traded to a given country
(assuming equal sex ratios). Fourth, the biogeographical realms used
in this study to filter trade transactions were adapted from Olson et al.
(42), and the Palearctic region was divided in western and eastern
regions following the study of Cramp and Simmons (43). All trading
countries were classified according to the realm to which they belong.
In the event that a country was crossed by a realm border, it was placed
in the realm that covers the largest area. Bird species were similarly
classified in terms of the biogeographical realm to which they are native.
If the native area covers more than one realm, the species was classified
as native to all of them. Last, we verified the agreement between importer
and exporter reported (log) quantities, and found that while agreement
was high before the EU trade ban (Pearsons r = 0.82; 95% CI, 0.76 to
0.86), larger discrepancies were apparent after the ban (r = 0.61; 95%
CI, 0.51 to 0.70). The slope of a linear regression between (log) export-
er and importer quantities was not different from the one before the
EU ban (slope, 0.93; 95% CI, 0.84 to 1.02), but it was after the ban
(slope, 0.63; 95% CI, 0.51 to 0.75). Post-ban CITES discrepancies
are illustrated as the difference between declared (log) exports and
imports in fig. S8.
Trade network metrics
On the basis of the CITES trade database, we derived several variables
relevant to species invasion risk from the global bird trade. First, for each
species, the annual total number of live, wild-caught birds that have
been (legally) exported to a given country in the periods 19952005
and 20062011 is given by the variable quantity. Second, to test our
hypothesis that wildlife trade determines species invasion risk not only
by increasing the number of individuals that are eventually introduced
to new ranges but also through specific features of the trade network,
we apply a set of network metrics that were developed within the
framework of graph theory (44). The trade network for the pre- and
post-ban period was created as a directed graph for each bird species
Reino et al., Sci. Adv. 2017; 3 : e1700783 22 November 2017
such that the nodes refer to countries and edges refer to the trade
observed between an exporter and an importer country. The weight of
the edge is represented by the quantity of birds traded. We selected the
following metrics to describe the topological properties of countries in
the trade network: indegree, closeness centrality, eigenvector centrality,
betweenness centrality, and clustering coefficient. The variable indegree
describes the number of incoming links (edges) to a country (node),
thus reporting the number of countries from which a certain country
imports birds. Closeness centrality indicates how closely connected a
country is to all other countries in the trade network, considering the
shortest path between countries. We calculated this metric on an
inverted networksource and target countries were swappedso that
the parameter measures the average of the number of steps in the trade
network between the exporter (source) and the importer (target)
country. The higher the value is, the more central (shortest distance)
the country is, that is, the shorter the trade routes of imported birds
are. The eigenvector centrality is another measure of the influence
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of a country in the trade network, and it computes the centrality of a
country based on the centrality scores of its connections. Thus, a
country is considered influential to a trade network (receives a high ei-
genvector centrality score) if it trades a lot with countries that are also
influential. Betweenness centrality reports how often a country is
found on a shortest path between two countries in the network, and
thus measures the extent to which the overall trade flow must pass
through a particular country or, in other words, a countrys gatekeeping
role. Last, the clustering coefficient measures the probability that the
trading partners of a country are connected, and higher values of the
coefficient indicate the presence of highly interconnected groups of
countries in the trade network. Trade metrics were not strongly
correlated to each other (all r < 0.64). To visualize changes in global
network structure before and after the EU bird trade ban, (standardized)
network parameter values were first summed per country to plot the
highest-ranking parameter (figs. S1 and S2). Trade networks and asso-
ciated statistics were obtained for each taxa, using a custom design
java application for this purpose (https://github.com/rpfigueira/
trademetrics) and the open-source Gephi Toolkit library (https://
gephi.org/toolkit/).
Non-native bird occurrence data
To be included in our data set, bird invasions to areas outside species
natural ranges had to comply with the following conditions. First, inva-
sions before 1995 were not included (because of CITES trade data set
limitations; see above). Second, bird invasions were considered success-
ful if a population was still reported as present at least 5 years after the
introduction event [introductions after the year 2011 were thus not
considered, sensu Chiron et al. (41)]. Third, and logically, only
CITES-listed bird species were considered. Fourth, island systems that
are not an independent party to CITES were excluded. Fifth, multiple
successful invasions of the same species to the same country were
considered as a single successful invasion of that country for that spe-
cies. Sixth, invasive bird populations that likely resulted from range ex-
pansion of species introduced to neighboring countries were not
retained. Last, as for the trade data, only species invasions across bio-
geographical realms were considered to discriminate anthropogenic
species introductions from possible natural (for example, climate
changedriven) range expansion. Of the 1470 birds species identified
up to the species level that are listed in the Index of CITES species
(http://checklist.cites.org), 566 species met these criteria. Bird invasion
events for these species were assessed and updated from previously
published databases, such as the European DAISIE database (41) and
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SCIENCE ADVANCES | RESEARCH ARTICLE
global databases on avian invasions compiled by Dyer et al. (19),
Lever (45), and Sol et al. (46). In addition, for each of the 566 species
retained, we searched Google Scholar with the search string invasive
OR non-native AND species scientific name using the time period
19952016. For each species, we checked the title and abstract of up
to the first 100 hits to decide whether the mentioned (scientific or gray
literature) report might hold information on introduction events to
non-native ranges. When uncertainty existed on the status of introduc-
tion events (that is, successful invasion or not), we searched for recent
species observations on the online databases eBird (http://ebird.
org), iNaturalist (www.inaturalist.org), and Global Biodiversity
Information Facility (www.gbif.org). In addition, we consulted a
leading bird trip report repository (www.cloudbirders.com). For 21 of
566 bird species complying with our inclusion criteria, we found
qualified, successful invasion events. In total, 42 (36 pre-ban versus
6 post-ban) successful invasion events were uncovered across 23 dif-
ferent countries (table S6).
Statistical analysis
We modeled the probability of each of the species traded in the period
19952005 establishing non-native populations in that period as a
function of the trade metrics described above, using a phylogenetic
generalized linear mixed model in a Bayesian framework. We applied
a probit model in MCMCglmm (47, 48), with invasion success or failure
as a binary response variable, and weak priors for all predictors treated
as fixed effects [that is, the trade metrics described above; prior struc-
ture as follows: R=list(V=1,fix=1), G=list(G1=list(V=1, nu=0.002),
G2 = list(V=1, nu=0.002))]. Note that because binary response varia-
bles do not provide enough information to estimate residual variance,
the residual variance has been fixed to 1 (47, 48). Location (that is,
country), species identity, and phylogeny were included as random
factors. We took the phylogeny from Jetz et al. (49). However, this source
does not provide a unique consensus tree, and following Rubolini et al.
(50), we downloaded 1000 trees from the http://birdtree.org site and sum-
marized the phylogenetic information into a 50% majority-rule consen-
sus tree. All variables were standardized before analyses. MCMCglmm
models were run for 50,000,000 iterations with a burn-in of 10,000 and
a thinning interval of 500. Model convergence and mixing were assessed
by ensuring that the effective sample size for all estimates was larger than
1000; in addition, we used the Heidelberg stationary test as implemented
in the R package coda (51) to verify whether sampled values come
from a stationary distribution. Variable selection was carried out using
the R MuMIn package (52), which ran all possible additive combinations
of fixed effect variables, ranking models based on DIC values (53). The
resulting best-supported (baseline) model was then projected onto the
20062011 trade network data to obtain estimates of wild bird trade
related invasion risk after the implementation of the EU ban. These
baseline model forecasts rely on stable response-to-predictor variable re-
lationships. Although measuring the stability of these relationships is not
currently possible because of the low number of successful post-ban in-
vasion events, our baseline model is calibrated on the wide, global-scale
heterogeneity in trade flows present before the ban. As the current, post-
ban global trade network is a subset of the pre-ban network (fig. S3), our
invasion risk forecasts do not extend beyond the parameter space in
which the baseline model was calibrated. To visualize invasion risks in
the pre- and post-ban periods, species fitted (pre-ban) or predicted
(post-ban) invasion probabilities were summed per country (figs. S3
and S4); changes in invasion risk were visualized as the difference in
summed pre- and post-ban probabilities (Fig. 3).
Reino et al., Sci. Adv. 2017; 3 : e1700783 22 November 2017
SUPPLEMENTARY MATERIALS
Supplementary material for this article is available at http://advances.sciencemag.org/cgi/
content/full/3/11/e1700783/DC1
table S1. CITES bird trade data before and after the 2005 EU ban.
table S2. Overview of the 10 highest-ranked countries in terms of network centrality measures.
table S3. Overview of network parameter values per biogeographical region.
table S4. Birds annually exported to different biogeographical realms.
table S5. Birds annually exported from different biogeographical realms.
table S6. Invasion events of CITES-listed species before and after the 2005 EU ban.
fig. S1. Highest-ranking trade volume/network structure parameters in the period 19952005.
fig. S2. Highest-ranking trade volume/network structure parameters in the period 19952005.
fig. S3. Histograms of network centrality measures in the period 19952005 versus 20062011.
fig. S4. Global wild bird tradedriven invasion risk in the period 19952005.
fig. S5. Global wild bird tradedriven invasion risk in the period 20062011.
fig. S6. Trade fluxes of CITES-listed passerine birds in the period 19952005.
fig. S7. Trade fluxes of CITES-listed Psittaciformes birds in the period 19952005.
fig. S8. Discrepancies between exporter- and importer-listed quantities of traded wild birds.
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Acknowledgments: We thank COST Action ES1304 (ParrotNet) for sponsoring discussions
contributing to the manuscript development. Funding: This study was funded by FEDER
Funds through the Operational Competitiveness Factors Program COMPETE, and by National
Funds through the Foundation for Science and Technology (FCT) within the framework of
project PTDC/AAG-GLO/0463/2014-POCI-01-0145-FEDER-016583. L.R. and C.C. acknowledge
support from the FCT through grants SFRH/BPD/93079/2013 and SFRH/BPD/84422/2012,
respectively. D.S. is funded by a Marie Skodowska-Curie Action (H2020-MSCA-IF-2015, grant
706318) and, together with M.B.A., acknowledges the Danish National Research Foundation
for support to the Center for Macroecology, Evolution and Climate (grant DNRF96). P.B.
was supported by EDP (Energias de Portugal) Biodiversity Chair. Author contributions: L.R.,
M.B.A., P.B., D.S., and R.F. designed the study. L.R. and R.F. extracted data from the CITES
database. R.F. calculated network topology and metrics variables. L.R. and D.S. gathered data
on bird invasion events. D.S. performed statistical analyses. D.S., L.R., M.B.A., P.B., and
C.C. led the manuscript writing. All authors contributed to interpreting the results and revising
the manuscript and approved the final manuscript. Competing interests: The authors
declare that they have no competing interests. Data and materials availability: The data that
support the findings of this study are made available in the supplementary tables and/or
can be freely downloaded at https://trade.cites.org/ and http://birdtree.org/.
Submitted 14 March 2017
Accepted 31 October 2017
Published 22 November 2017
10.1126/sciadv.1700783
Citation: L. Reino, R. Figueira, P. Beja, M. B. Arajo, C. Capinha, D. Strubbe, Networks of global
bird invasion altered by regional trade ban. Sci. Adv. 3, e1700783 (2017).
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Networks of global bird invasion altered by regional trade ban
Lus Reino, Rui Figueira, Pedro Beja, Miguel B. Arajo, Csar Capinha and Diederik Strubbe

Sci Adv 3 (11), e1700783.

DOI: 10.1126/sciadv.1700783

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